A mechanism for differential control of axonal and dendritic spiking underlying learning in a cerebellum-like circuit

Abstract

In addition to the action potentials used for axonal signaling, many neurons generate dendritic "spikes" associated with synaptic plasticity. However, in order to control both plasticity and signaling, synaptic inputs must be able to differentially modulate the firing of these two spike types. Here, we investigate this issue in the electrosensory lobe (ELL) of weakly electric mormyrid fish, where separate control over axonal and dendritic spikes is essential for the transmission of learned predictive signals from inhibitory interneurons to the output stage of the circuit. Through a combination of experimental and modeling studies, we uncover a novel mechanism by which sensory input selectively modulates the rate of dendritic spiking by adjusting the amplitude of backpropagating axonal action potentials. Interestingly, this mechanism does not require spatially segregated synaptic inputs or dendritic compartmentalization but relies instead on an electrotonically distant spike initiation site in the axon-a common biophysical feature of neurons.